Elsevier

NeuroImage

Volume 30, Issue 4, 1 May 2006, Pages 1357-1364
NeuroImage

Gamma-band activity dissociates between matching and nonmatching stimulus pairs in an auditory delayed matching-to-sample task

https://doi.org/10.1016/j.neuroimage.2005.11.010Get rights and content

Abstract

Electro- and magnetoencephalography studies have suggested that increased gamma-band activity (GBA) is a correlate of activated neural stimulus representations. In this study, a delayed matching-to-sample paradigm for auditory spatial information was employed to investigate the role of magnetoencephalographic gamma-band activity in the differentiation between matching and nonmatching stimulus pairs. Twelve subjects made same–different judgments about the lateralization angle of pairs of filtered noise stimuli (S1 and S2) presented with 0.8-s delays. One half of the subjects had to respond to matching stimulus pairs, the other half to nonmatching stimulus pairs. Cortical oscillatory activity in the memory task was compared to a control task requiring the detection of background noise intensity changes. Memory-related GBA increases were revealed over midline parietal areas in the middle of the delay phase and during the presentation of S2 and over frontocentral areas at the end of the delay phase. This replicated previous findings. In addition, nonmatching trials were associated with increased GBA over right parietal areas in response to S2. The midline parietal GBA increase during S2 in the memory condition may have reflected the representation of S1 needed for a comparison between S1 and S2. When S1 and S2 were identical, no further representation was required. In contrast, for nonmatching pairs, a second representation was activated over right parietal areas.

Introduction

Working memory refers both to the maintenance of information in the absence of sensory input and to operations on this information that serve to perform goal-directed behavior (Baddeley and Hitch, 1974). Single-cell recordings in monkeys (Compte et al., 2003, Fuster and Alexander, 1971, Lee et al., 2005), electromagnetic (Croizé et al., 2004, Gevins et al., 1997, Mecklinger and Pfeifer, 1996) and hemodynamic brain imaging studies (Jonides et al., 1993, Klingberg et al., 1997, Owen et al., 1999) have supported the notion that working memory is mediated by a network comprising prefrontal and posterior brain regions. In the auditory modality, Martinkauppi et al. (2000) found hemodynamic activations in parietal and prefrontal regions in a spatial working memory paradigm. Alain et al. (2001) reported increased hemodynamic activity in posterior temporal, parietal and superior frontal regions in an auditory delayed matching-to-sample task for sound location. While posterior brain regions are thought to be engaged in the storage of sensory stimuli, prefrontal areas are supposed to be involved in the maintenance or manipulation of these sensory stimuli (Curtis and D'Esposito, 2003, Petrides, 2000).

As much as hemodynamic techniques tell us about the topography of regions involved in working memory, they provide little information about the temporal dynamics of the underlying neural activations. Recently, there has been increasing evidence that cognitive processes are related to synchronized oscillatory activity of neurons organized in distributed cell assemblies (Varela et al., 2001, Ward, 2003). Oscillatory brain activity as a measure of the dynamics of cognitive processes can be studied with electroencephalography (EEG) or magnetoencephalography (MEG). EEG and MEG studies point to a role of induced oscillatory activity in the gamma-band range (above 30 Hz) in working memory (for reviews, see Kaiser and Lutzenberger, 2003, Kaiser and Lutzenberger, 2005, Tallon-Baudry and Bertrand, 1999). In EEG, enhanced gamma-band activity (GBA) has been found at occipitotemporal and frontocentral electrodes during the delay phase of a visual delayed matching-to-sample (DMTS) task compared to a task not requiring memory processes (Tallon-Baudry et al., 1998). The occipitotemporal GBA enhancement has been interpreted as a correlate of the synchronization of a cortical network representing the visual stimulus, whereas the frontocentral increase may have indicated active maintenance processes. While GBA effects in EEG typically show a rather broad topography and frequency spectrum (24–60 Hz), in MEG, effects have been found to be more spectrally and topographically narrow (Kaiser et al., 2003, Lutzenberger et al., 2002). The topography of these effects corresponds well with findings from hemodynamic brain imaging studies (Alain et al., 2001), supporting a possible link between oscillatory activity and the blood-oxygen-level-dependent effect (Foucher et al., 2003, Logothetis et al., 2001).

During an auditory spatial working memory task requiring same–different judgments about the lateralization of two filtered noise stimuli S1 and S2, we have found enhanced GBA over posterior parietal cortex at ∼59 Hz in the middle of the 0.8-s delay period (Lutzenberger et al., 2002). At the end of the delay phase and during the presentation of S2, enhanced GBA at ∼67 Hz was observed over right frontal cortex and later over midline parietal areas. We have interpreted the posterior parietal enhancement at ∼59 Hz as reflecting the representation of S1 based on synchronization of networks belonging to the putative auditory dorsal stream. This stream is thought to be involved in auditory spatial processing (Arnott et al., 2004, Kaas et al., 1999, Kaiser et al., 2000a, Kaiser et al., 2000b, Kaiser et al., 2002, Rauschecker and Tian, 2000). The GBA increase over right frontal cortex at ∼67 Hz could indicate preparation for the comparison of S1 and S2, whereas the increase over midline parietal areas in the same frequency band could be associated with the representation of S2. However, the latter spectral amplitude enhancement can only be interpreted with caution since only nonmatching S1–S2 pairs were analyzed in this study.

The aim of the present study was to assess the neuromagnetic correlates of the differentiation between matching and nonmatching stimulus pairs. Here, we followed the paradigm used in our previous auditory spatial working memory study (Lutzenberger et al., 2002) but presented equal numbers of matching and nonmatching stimulus pairs. In keeping with the notion of GBA as a correlate of activated neural representations, we expected an additional component of enhanced GBA in response to S2 if S2 differed from S1. In addition, we aimed to replicate the pattern of posterior parietal and frontal GBA increases found in our previous auditory spatial working memory study.

Section snippets

Participants

The sample comprised of twelve volunteers (eight females; mean age: 24.75, SD = 2.67) from the University of Tübingen and the surrounding community. All participants gave written informed consent and were paid 10. The study was approved by the ethics committee of the University of Tübingen Medical Faculty.

Procedure and stimulus material

Subjects were seated upright in a magnetically shielded room (Vakuum-Schmelze, Hanau, Germany). They were instructed to sit still and keep their eyes open, looking at a fixation cross in the

Behavioral data

Subjects showed an overall performance of 68.63% hits (SD = 12.34) and 82.99% correct rejections (SD = 13.63) for the memory condition and 62.02% hits (SD = 14.42) and 92.51% correct rejections (SD = 7.38) for the control condition. These data are comparable to the performance results that were obtained in a previous auditory spatial working memory task (Lutzenberger et al., 2002). Hit rate and correct rejection rate for the matching memory trials were 67.49% (SD = 13.83) and 83.33%

Discussion

The present study investigated induced oscillatory activity in human MEG during auditory spatial working memory. The main focus of the study was on the differentiation between matching and nonmatching stimulus pairs. A delayed matching-to-sample task was used in which one half of the subjects had to respond to matching stimulus pairs, while the other half responded to nonmatching stimulus pairs. This enabled the comparison of nonmatching and matching stimulus pairs without confounding memory-

Acknowledgment

This work was supported by Deutsche Forschungsgemeinschaft (SFB 550/C1).

References (48)

  • A. Mecklinger et al.

    Event-related potentials reveal topographical and temporal distinct neuronal activation patterns for spatial and object working memory

    Brain Res. Cogn. Brain Res.

    (1996)
  • F. Pulvermüller et al.

    High-frequency brain activity: its possible role in attention, perception and language processing

    Prog. Neurobiol.

    (1997)
  • J. Quintana et al.

    Prefrontal representation of stimulus attributes during delay tasks: I. Unit activity in cross-temporal integration of sensory and sensory–motor information

    Brain Res.

    (1988)
  • C. Tallon-Baudry et al.

    Oscillatory gamma activity in humans and its role in object representation

    Trends Cogn. Sci.

    (1999)
  • L.M. Ward

    Synchronous neural oscillations and cognitive processes

    Trends Cogn. Sci.

    (2003)
  • C. Alain et al.

    “What” and “where” in the human auditory system

    Proc. Natl. Acad. Sci. U. S. A.

    (2001)
  • A. Baddeley

    Working memory: looking back and looking forward

    Nat. Rev., Neurosci.

    (2003)
  • A.D. Baddeley et al.

    Working memory

  • R.C. Blair et al.

    An alternative method for significance testing of waveform difference potentials

    Psychophysiology

    (1993)
  • M. Bodner et al.

    Auditory memory cells in dorsolateral prefrontal cortex

    NeuroReport

    (1996)
  • A. Compte et al.

    Temporally irregular mnemonic persistent activity in prefrontal neurons of monkeys during a delayed response task

    J. Neurophysiol.

    (2003)
  • R. Elliott et al.

    Differential neural responses during performance of matching and nonmatching to sample tasks at two delay intervals

    J. Neurosci.

    (1999)
  • J.R. Foucher et al.

    The BOLD response and the gamma oscillations respond differently than evoked potentials: an interleaved EEG–fMRI study

    BMC Neurosci.

    (2003)
  • J.M. Fuster et al.

    Neuron activity related to short-term memory

    Science

    (1971)
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